Coexistence of Anaemia and Stunting among Children Aged 6–59 Months in Ethiopia: Findings from the Nationally Representative Cross-Sectional Study

Introduction: Stunting and anaemia, two severe public health problems, affect a significant number of children under the age of five. To date, the burden of and predictive factors for coexisting forms of stunting and anaemia in childhood have not been well documented in Ethiopia, where both the conditions are endemic. The primary aims of the present study were to: (i) determine the prevalence of co-morbid anaemia and stunting (CAS); (ii) and identify factors associated with these co-morbid conditions among children aged 6–59 months in Ethiopia. Methods: The study was based on data from the Ethiopian Demographic and Health Survey (EDHS 2005–2016). The EDHS was a cross-sectional study that used a two-stage stratified cluster sampling technique to select households. A total weighted sample of 21,172 children aged 6–59 months was included in the current study (EDHS-2005 (n = 3898), EDHS-2011 (n = 8943), and EDHS-2016 (n = 8332)). Children with height-for-age z-scores (HAZ) less than −2 SD were classified as stunted. Anaemia status was measured by haemoglobin level with readings below 11.0 g/deciliter (g/dL) categorized as anaemic. A multilevel mixed-effects logistic regression model was used to identify the factors associated with CAS. The findings from the models were reported as adjusted odds ratios (AOR) with 95% confidence intervals (CIs). Results: Almost half of the children were males (51.1%) and the majority were from rural areas (89.2%). The prevalence of CAS was 24.4% [95% CI: (23.8–24.9)]. Multivariate analyses revealed that children aged 12–23 months, 24–35 months, and 36–59 months, and children perceived by their mothers to be smaller than normal at birth had higher odds of CAS. The odds of CAS were significantly higher among children born to anaemic mothers [AOR: 1.25, 95% CI: (1.11–1.41)], mothers with very short stature [AOR: 2.04, 95% CI: (1.44–2.91)], children from households which practiced open defecation [AOR: 1.57, 95% CI: (1.27–1.92)], children born to mothers without education [AOR: 3.66, 95% CI: (1.85–7.22)], and those who reside in rural areas [AOR: 1.41, 95% CI: (1.10, 1.82)]. Male children had 19% lower odds of having CAS compared to female children [AOR: 0.81, 95% CI: (0.73–0.91)]. Children born to mothers who had normal body mass index (BMI) [AOR: 0.82, 95%CI: (0.73–0.92)] reported lower odds of CAS. Conclusions: One in four preschool-age children in Ethiopia had co-morbid anaemia and stunting, which is a significant public health problem. Future interventions to reduce CAS in Ethiopia should target those children perceived to be small at birth, anaemic mothers, and mothers with short stature.


Introduction
Undernutrition is one of the significant public health scourges that particularly affects young children [1], and around 45% of deaths among children under 5 years of age are The study used data from the Ethiopian Demographic and Health Survey (EDHS) from 2005 to 2016 [23][24][25]. The EDHS was a cross-sectional study that employed a two-stage stratified cluster sampling technique to select households. The sampling procedure has been described in detail in the EDHS report [23][24][25]. For this study, 21,172 children's data from the EDHS (2005-2016) documents were obtained and used for this secondary analysis, with a complete response to all variables of interest (Supplementary File S1).

Data Collection
The EDHS gathered information on children's nutritional status by measuring the weight and height of children under the age of five in all sampled households. Height was measured with a measuring board (i.e., ShorrBoard Portable height length measurement board). Children younger than the age of 24 months were measured lying down on the board (recumbent length) while standing height was measured for older children [23]. The EDHS also collected blood samples from all children aged 6 to 59 months who participated in the survey for haemoglobin tests. Haemoglobin analysis was carried out on-site using a battery-operated portable HemoCue analyzer, Angelholm, Sweden (HemoCue ® ). Blood samples were drawn from a drop of blood taken from a finger prick. Children with a haemoglobin level of less than 11 g/dL were considered anaemic [23][24][25].
The EDHS collected anthropometric data on height and weight for women age 15-49 who were not pregnant. These data were used to calculate maternal body mass index (BMI). The BMI was calculated by dividing weight in kilograms by height in metres squared (kg/m 2 ). Maternal BMI was classified as underweight (<18.5 kg/m 2 ), normal (18.5 to <24.9 kg/m 2 ), or overweight/obesity ≥ 25.0 kg/m 2 ) [23].
Anaemia among women age 15-49 was measured by the HemoCue instrument capillary blood, and was collected exclusively from a finger prick. A hemoglobin level of less than 11 g/dL was categorized as anaemia for non-pregnant women [23,26].

Variable and Measurements
Concurrent stunting and anaemia (CAS) was our primary outcome, defined as the child having a simultaneous presence of both anaemia and stunting conditions [10,11]. All children with height-for-age z-scores (HAZ) less than −2 standard deviations (SD) were classified as stunted [27] and a haemoglobin level < 11.0 g/deciliter was categorized as anaemia [26].

Independent Variable
Potential factors of CAS in children were extracted from the EDHS dataset. The factors were also selected based on previous studies [6,7,10,11]. The identified factors were categorized into individual, household, and community-level factors. A detailed list and variable coding of all independent variables are presented in Supplementary File S2.

Data Analysis
All analyses were carried out using STATA/MP version 14.1 (StataCorp, College Station, TX, USA) to adjust for clusters and survey weights. Sampling weighting was applied to all descriptive statistics to compensate for the disproportionate allocation of the sample [23]. Multilevel logistic regression models were used to determine communityand individual-level factors associated with CAS. A bivariable multilevel analysis was first performed to identify factors associated with CAS. Potential factors with a p-value < 0.2 obtained in the multilevel bivariable analysis were selected to enter multilevel multivariable logistic regression models to estimate their independent association with the outcome variable. Four models were fitted and an empty model without any explanatory variables was run to detect the presence of a possible contextual effect; the first with individuallevel variables (model I), the second with household-level variables (model II), the third with community-level variables (model III), and the fourth with individual-, household-, and community-level variables (model IV). The intraclass correlation coefficient (ICC) was computed for each model to show the variations explained at each level of modelling. Model comparisons were performed using the deviance information criteria (DIC), Akaike information criteria (AIC), and Bayesian information criteria (BIC). The model with the lowest DIC, AIC, and BIC, was considered the best-fit model. Finally, the fourth model (model IV) with the lowest information criteria value was chosen as the final best-fit model.

Sociodemographic Characteristics of the Sample
A total of 21,172 children aged 6-59 months were included in the study (EDHS-2005 (n = 3898), EDHS-2011 (n = 8943), and EDHS-2016 (n = 8332)) and the majority were from rural areas (89.2%). Almost half of the children were males (51.1%). Nearly half of the children (45.9%) were in the age group of 36-59 months and 21% were between the ages of 12-23 and 14-35 months. The majority of the children (70.5%) were currently breastfeeding. Of all the study participants, 14,862 (70.2%) were born to mothers who were not educated, 45.5% were from poor households, 21.0% were from middle wealth quantiles, and 33.5% were from the richest households (Table 1).

Prevalence of Anaemia, Stunting, and Concurrent Anaemia and Stunting (CAS)
The prevalence of stunting and anaemia was found to be 43.1% ( The prevalence of CAS varied by gender, with males accounting for 54.0% of those affected. About 41.9% of CAS children were between 36 and 59 months. The proportion of children with CAS was higher among uneducated mothers (75.1%), and in mothers who did not attend ANC (57.1%). The children from the poorest households (52.9%) and the children living in rural regions had a higher prevalence of CAS (93.6%). The detailed prevalence by different factors is given in Table 2.

Prevalence of Anaemia, Stunting, and Concurrent Anaemia and Stunting (CAS)
The prevalence of stunting and anaemia was found to be 43.1%  The prevalence of CAS varied by gender, with males accounting for 54.0% of those affected. About 41.9% of CAS children were between 36 and 59 months. The proportion of children with CAS was higher among uneducated mothers (75.1%), and in mothers who did not attend ANC (57.1%). The children from the poorest households (52.9 %) and the children living in rural regions had a higher prevalence of CAS (93.6%). The detailed prevalence by different factors is given in Table 2.      The odds of having CAS among children from households that cooked outdoors [AOR: 0.82, 95% CI: (0.69-0.97)] was lower than children from households that cooked in the house. At the community level, the odds of CAS were higher among those residing in rural areas [AOR: 1.41, 95% CI: (1.10, 1.82)] than urban dwellers. The odds of having CAS among children from large central regions were lower compared with children in the metropolis area [AOR: 0.79, 95% CI: (0.63-0.98)] (Table 3).

Discussion
The present study was mainly designed to elucidate the prevalence of co-morbid anaemia and stunting (CAS), and its associated factors, among children aged 6-59 months. To our knowledge, no study in Ethiopia has examined the coexisting forms of CAS using a country-wide pooled dataset. In Ethiopia, the prevalence of CAS was found to be 24.40%. The factors associated with increased odds of CAS include older child age, children reported to be smaller than normal at birth, children born from anaemic mothers, children born to mothers with short or very short stature, children born to mothers with normal weight or overweight/obese, and children born to mothers with no education. In addition, higher odds of CAS were reported among children from households that practiced open defecation and those living in rural areas.
This study reported a 24.4% prevalence of CAS, which was comparable with a previous study conducted in Ethiopia that reported a 23.9% prevalence [11]. This finding implies that CAS in Ethiopia is a major public health concern, as it affects one in every four children under the age of five years. Several explanations are plausible for the higher prevalence of CAS in under-five-year-olds in Ethiopia. Firstly, both stunting and anaemia have been reported to be the most prevalent conditions in Ethiopia. The national prevalence of stunting was 38% and more than half (57%) of Ethiopian children aged 6-59 months are anaemic [23]. Secondly, Ethiopian poor dietary patterns and poor food security may explain the high prevalence of concurrent undernutrition and micronutrient deficiencies. According to an Ethiopian study, food-insecure households may have limited access to a diverse range of nutritious foods and have low meal frequencies, which increase the co-occurrence of stunting and anaemia due to overall low nutrient intakes [11].
The finding on the current prevalence of CAS was slightly higher than the 21.5% reported in a study conducted in forty-three LIMICs among younger children aged 6 to 59 months [6], and the observed co-occurrence of 22% among Indian children aged 6-18 months [7]. Additionally, the prevalence found in this study was higher than that reported in a community-based cross-sectional survey conducted in Southern Ethiopia, where 17.8% [10] and 10.5% had CAS [22], and than the 5.94% reported in Maracaibo, Venezuela [9]. This variation could be attributed to the study design and sample size, as we used national data sources.
In this study, the odds of experiencing CAS were lower among male children in comparison to females. However, other studies have reported higher odds of CAS in boys than girls [11,28]. This could be explained, in part, by the difference in the study population, as the previous two studies included children aged 6-24 months in their analysis. The role of sex varies across places, and its relationship with the burden of CAS requires further investigation.
Our finding reported higher odds of CAS in older children than in their younger counterparts which concurred with previous reports, which consistently demonstrated higher risks of CAS as the children's age increased [10,11]. The data from the current study confirmed the lower odds of comorbid anaemia and stunting in children whose mothers have normal BMI than those born to underweight mothers. This finding indicates that children born to mothers with normal BMIs are less likely to experience anaemia, stunting, or CAS. A prior prospective cohort study in China on maternal BMI during early pregnancy with infant anaemia showed that maternal BMI during early pregnancy is correlated with infant haemoglobin in an inverse U-shaped profile [29]. Underweight mothers are more likely to have a stunted child, and stunted children are more likely to be anaemic, due to the intergenerational cycle of stunting. Supporting this assertion, a Brazilian study found positive correlations between haemoglobin (Hb) levels and HAZ, even after controlling for age [30], which ultimately led to CAS. Furthermore, Afolabi and Palamuleni reported that the likelihood of stunting was higher among anaemic children [31]. Likewise, the study identified children born of anaemic mothers and mothers with short/very short stature as being significantly associated with higher odds of childhood CAS. Various earlier studies have reported that the odds of stunting are higher among children of mothers with short stature [32][33][34], which may be a plausible reason for higher CAS. Moreover, the reported intergenerational cycle of malnutrition, in which stunted female children grow to become stunted mothers, who give birth to stunted children, may explain the relationship [35]. The current study also found that children who were reported to be smaller than normal at birth, and those from households with open defecation, had a higher risk of CAS. These findings were consistent with the existing literature, demonstrating that a small birth size is associated with a higher risk of CAS than a large birth size [11]. In the current study, children from households practicing open defecation had increased odds of having CAS. The association between anaemia and/or stunting and open defecation could have many plausible explanations, including being caused by intestinal parasite infections and environmental enteropathy [36][37][38][39][40].
The odds of having CAS among children from households that cooked outdoors was lower than children from households that cooked in the house. We hypothesis that, in a country where a significant number of households used solid fuel and no in-house potable water, cooking outdoors could pose a lower risk of indoor air pollution and indoor contaminations due to an enclosed space and a lack of running water. Other studies have demonstrated that the likelihood of anaemia was higher among children from households that used solid fuels; biofuel smoke contains significant amounts of carbon monoxide [41,42].
In the current study, the education level of the mother was also associated with CAS. For example, mothers with no education, and those with primary and secondary education were associated with higher odds of CAS compared with those with higher than secondary level education. This finding is also consistent with previous studies that found no or low maternal education status to be associated with several poor nutritional outcomes [6,7,11].
Additionally, among the current study findings, children living in rural areas had higher odds of having CAS than those living in urban areas. This finding aligns with previous double-burden studies that showed living in rural areas to be strongly associated with co-morbidities [6,43]. People in rural areas are often at a disadvantage in terms of living conditions, economic status, and access to health care and other social services across many LMICs.
The study has some limitations. Firstly, the analyses were conducted using EDHS data collected in a cross-sectional survey, which prevents causal inferences. Secondly, because of the self-reported nature of the inquiry, there is a possibility of recall bias. Thirdly, due to the secondary nature of the data, the present study was limited by unmeasured confounders.

Conclusions
One in every four children in Ethiopia is affected by CAS, making it a significant public health problem. Stunting, anaemia, and their co-occurring health conditions have created a syndemic situation in Ethiopia situation whereby two or more factors are likely to work together to exacerbate a health crisis. Both individual-level (older children, children perceived by their mother to be smaller than normal at birth, children born to anaemic mothers, mothers with short or very short stature, low maternal education, and children from households with open defecation) and community-level factors (place of residency) were revealed to be important factors for CAS in Ethiopia. While the prevalence of CAS was lower among male children, children born from mothers with BMIs (kg/m 2 ) of 18.5 to 24.9 and 25 and above, children born by mothers with BMIs lower that 18.5 kg/m 2 , and children born from mothers who were anaemic were likely to have CAS. Thus, intervention programs aiming to prevent anaemia and stunting should also consider addressing both burdens simultaneously by identifying individual-and contextual-level factors.  Institutional Review Board Statement: Ethical review and approval were waived for this study, due to the data being publicly available in an open access repository (http://dhsprogram.com/data/ available-datasets.cfm (accessed on 28 March 2022)) and being anonymised. The data were obtained via online registration to measure the DHS program and were downloaded after the purpose of the analysis was communicated and approved. An approval letter for the use of the EDHS data set was gained from Measure DHS.

Informed Consent Statement:
Participants' informed consent was not required for this analysis, as data were anonymised and obtained from secondary sources.

Data Availability Statement:
The datasets analysed during the current study are publicly available on the Measure DHS website https://dhsprogram.com/data/dataset_admin/login_main.cfm (accessed on 28 March 2022), after formal online registration and submission of the project title and detailed project description.